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Ramping activity in midbrain dopamine neurons signifies the use of a cognitive map

View ORCID ProfileAkash Guru, View ORCID ProfileChangwoo Seo, View ORCID ProfileRyan J. Post, Durga S. Kullakanda, Julia A. Schaffer, View ORCID ProfileMelissa R. Warden
doi: https://doi.org/10.1101/2020.05.21.108886
Akash Guru
1Department of Neurobiology and Behavior, Cornell University, Ithaca NY 14853 USA
2Cornell Neurotech, Cornell University, Ithaca NY 14853 USA
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  • ORCID record for Akash Guru
Changwoo Seo
1Department of Neurobiology and Behavior, Cornell University, Ithaca NY 14853 USA
2Cornell Neurotech, Cornell University, Ithaca NY 14853 USA
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Ryan J. Post
1Department of Neurobiology and Behavior, Cornell University, Ithaca NY 14853 USA
2Cornell Neurotech, Cornell University, Ithaca NY 14853 USA
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Durga S. Kullakanda
1Department of Neurobiology and Behavior, Cornell University, Ithaca NY 14853 USA
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Julia A. Schaffer
1Department of Neurobiology and Behavior, Cornell University, Ithaca NY 14853 USA
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Melissa R. Warden
1Department of Neurobiology and Behavior, Cornell University, Ithaca NY 14853 USA
2Cornell Neurotech, Cornell University, Ithaca NY 14853 USA
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  • For correspondence: mrwarden@cornell.edu
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Abstract

Journeys to novel and familiar destinations employ different navigational strategies. The first drive to a new restaurant relies on map-based planning, but after repeated trips the drive is automatic and guided by local environmental cues1,2. Ventral striatal dopamine rises during navigation toward goals and reflects the spatial proximity and value of goals3, but the impact of experience, the neural mechanisms, and the functional significance of dopamine ramps are unknown4,5. Here, we used fiber photometry6–8 to record the evolution of activity in midbrain dopamine neurons as mice learned a variety of reward-seeking tasks, starting recordings before training had commenced and continuing daily for weeks. When mice navigated through space toward a goal, robust ramping activity in dopamine neurons appeared immediately – after the first rewarded trial on the first training day in completely naïve animals. In this task spatial cues were available to guide behavior, and although ramps were strong at first, they gradually faded away as training progressed. If instead mice learned to run a fixed distance on a stationary wheel for reward, a task that required an internal model of progress toward the goal, strong dopamine ramps persisted indefinitely. In a passive task in which a visible cue and reward moved together toward the mouse, ramps appeared and then faded over several days, but in an otherwise identical task with a stationary cue and reward ramps never appeared. Our findings provide strong evidence that ramping activity in midbrain dopamine neurons reflects the use of a cognitive map9,10 – an internal model of the distance already covered and the remaining distance until the goal is reached. We hypothesize that dopamine ramps may be used to reinforce locations on the way to newly-discovered rewards in order to build a graded ventral striatal value landscape for guiding routine spatial behavior.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted May 22, 2020.
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Ramping activity in midbrain dopamine neurons signifies the use of a cognitive map
Akash Guru, Changwoo Seo, Ryan J. Post, Durga S. Kullakanda, Julia A. Schaffer, Melissa R. Warden
bioRxiv 2020.05.21.108886; doi: https://doi.org/10.1101/2020.05.21.108886
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Ramping activity in midbrain dopamine neurons signifies the use of a cognitive map
Akash Guru, Changwoo Seo, Ryan J. Post, Durga S. Kullakanda, Julia A. Schaffer, Melissa R. Warden
bioRxiv 2020.05.21.108886; doi: https://doi.org/10.1101/2020.05.21.108886

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